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Journal of Maxillofacial & Oral Surgery logoLink to Journal of Maxillofacial & Oral Surgery
. 2018 Aug 2;18(2):180–189. doi: 10.1007/s12663-018-1139-7

Systematic Review of Lesser Known Parasitoses: Maxillofacial Dirofilariasis

Kirti Chaudhry 1, Shruti Khatana 2,✉, Naveen Dutt 3, Yogesh Mittal 4, Shailja Sharma 5, Poonam Elhence 6
PMCID: PMC6441424  PMID: 30996536

Abstract

Background

Dirofilariasis is an endemic disease in tropical and subtropical countries caused by about 40 different species of dirofilari. Dirofilariasis of the oral cavity is extremely rare and is usually seen as mucosal or submucosal nodules. We also present a case of dirofilariasis of the mandibular third molar region submucosally in a 26 year old male patient.

Purpose

To identify, enlist and analyze the cases of dirofilariasis in maxillofacial region reported worldwide so as to understand the clinical presentation and encourage the consideration of helminthic infections as a possible differential diagnosis in maxillofacial swellings.

Methods

Two authors KC and SK independently searched the electronic database of PUBMED, OVID, Google Scholar and manual search from other sources. A general search strategy was planned and anatomic areas of interest identified. The search was made within a bracket of 1 month by the independent authors KC and SK who assessed titles, abstracts and full texts of articles based on the decided keywords. The final selection of articles was screened for the cases that were reported in the maxillofacial region including the age, gender, site of occurrence and region of the world reported in. A geographic distribution of the reported cases was tabulated.

Results

A total number of 265, 97, 1327, 3 articles were identified by PubMed, Ovid, GoogleScholar and manual search respectively. The final articles were manually searched for duplicates and filtered according to the inclusion/exclusion criteria which led to a final list of 58 unique articles that were included in the study. In total 99 cases were identified.

Conclusion

Although intraoral dirofilarial infections are extremely uncommon, it should be considered in the differential diagnosis of an intraoral or facial swelling that does not completely respond to routine therapy especially in patients from endemic areas.

Keywords: Dirofilariasis, Maxillofacial, Parasitosis, Diro, Filariasis

Introduction

Dirofilariasis is an endemic disease in tropical and subtropical countries caused by about 40 different species of Dirofilaria [1]. Dirofilaria is primarily confined to animals such as dogs, cats, foxes, raccoons and other wild animals which act as their definitive hosts. Humans are accidental or dead-end host and are infected by less than six species of Dirofilaria that too most commonly by Dirofilaria repens and Dirofilaria immitis [2].

Dirofilaria infection in humans characteristically manifests as a strong inflammatory reaction in the surrounding tissues and may have a varied clinical presentation depending on the site of infestation. Dirofilariasis of the oral cavity is extremely rare and is usually seen as mucosal or submucosal nodules. We present a case of dirofilariasis of the mandibular third molar region submucosally in a 26-year-old male patient.

Case Report

A 26-year-old male patient reported with a complaint of recurrent episodes of pain and swelling over the right side of lower face to the Department of Dentistry, All India Institute of Medical Sciences, Jodhpur, Rajasthan. Patient had three episodes of pain and swelling over the duration of 6 months. Extra orally, diffuse swelling of the right cheek was noted without any paresthesia. No cervical or generalized lymphadenopathy was present. Intraorally, pericoronitis and pus discharge around impacted right lower third molar were found (Fig. 1). An orthopantomograph revealed a distoangular impacted mandibular third molar with a small cystic radiolucency around the tooth (Fig. 2). Considering pericoronitis, surgical removal of third molar was planned under local anesthesia and antibiotics. During mucoperiosteal flap reflection, complete loss of periosteum with significant induration of the flap and slight erosion of underlying bone was seen. Suspecting some abnormal mass, procedure was deferred, an incisional biopsy was performed and specimen was sent for histopathological examination. Microscopic examination revealed edematous and inflamed granulation tissue with a profile of a single coiled unsheathed nematode within fibrocartilaginous tissue suggestive of Dirofilaria (Fig. 3).

Fig. 1.

Fig. 1

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Intraoral view

Fig. 2.

Fig. 2

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OPG view showing bone erosion distal to 48 

Fig. 3.

Fig. 3

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Histopathological report showing profile of a single coiled unsheathed nematode within fibrocartilaginous tissue

Patient’s chest X-ray ruled out any “coin lesions,” which characterize the lymphatic spread to lungs. Blood investigations revealed slightly raised erythrocyte sedimentation rate without any eosinophilia. Under antibiotic coverage, surgical removal of impacted right third molar along with excision of remaining inflamed granulation tissue around third molar was done. Antihelminthic drugs diethylcarbamazine (DEC) 100 mg thrice a day for three weeks, albendazole 400 mg once a day for 1 week and single dose of tablet ivermectin 12.5 mg were prescribed. Patient is on a regular follow-up since 36 months and is completely asymptomatic.

Aim

To identify, enlist and analyze the cases of dirofilariasis in maxillofacial region reported worldwide so as to understand the clinical presentation and encourage the consideration of helminthic infections as a possible differential diagnosis in maxillofacial swellings.

Materials and Methods

Two authors KC and SK independently searched the electronic database of PUBMED, OVID, Google Scholar and manual search from other sources. A general search strategy was planned, and anatomic areas of interest identified. There was no time bracket limitation for the search. The inclusion/exclusion criteria were identified as follows:

Inclusion Criteria

  • Cases diagnosed histopathologically or serologically as Dirofilaria

  • Cases in maxillofacial region in human beings only

  • Details of case available

  • English language/translated articles only

Exclusion criteria

  • Nematodes other than Dirofilaria

  • Non-human cases

  • Non-English language/translated articles only

  • Sites other than maxillofacial region or site details not available

The search was made within a bracket of 1 month by the independent authors KC and SK who assessed titles, abstracts and full texts of articles based on the following keywords: maxilla, mandible, jaw, zygomatic, zygoma, zygomaticotemporal, zygomatico-temporal, palate, palatal, subcutaneous, submucosal, dermal, face, facial, maxillofacial, oral cavity, mouth, cheek, buccal mucosa, buccinators, tongue, medial pterygoid, lateral pterygoid, pterygoid, masseter, temporalis, gum, gingiva, lip, parotid, submandibular, lingual, sublingual, nasolabial, labial, infraorbital with Dirofilaria, diro, dirofilariasis, helminth, nematode, and humans.

Titles that did not get excluded based on the exclusion criteria were selected for assessment of abstract or full text. Any disagreement was discussed on, and final selection made based on the inclusion and exclusion criteria. In addition, references of review articles were used as a retrospective database for articles which were manually handsearched.

The final selection of articles was screened for the cases that were reported in the maxillofacial region including the age, gender, site of occurrence and region of the world reported in. A geographic distribution of the reported cases was tabulated (Figs. 4, 5, 6, 7).

Fig. 4.

Fig. 4

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The world distribution of maxillo-mandibular dirofilariasis

Fig. 5.

Fig. 5

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Year wise distribution

Fig. 6.

Fig. 6

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Age affected

Fig. 7.

Fig. 7

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Site distribution

Results

Paper Selection

A total number of 265, 97, 1327 and 3 articles were identified by PubMed, Ovid, Google Scholar and manual search, respectively. The final articles were manually searched for duplicates and filtered according to the inclusion/exclusion criteria which led to a final list of 58 unique articles that were included in the study (Fig. 8).

Fig. 8.

Fig. 8

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Prisma diagram

Details

We checked the references of these articles for other cases and thoroughly studied them. Non-English literature has not been included in our review. Reviews by Avdiukhina et al. [3] and Ilyasov et al. [4] helped us to include cases published in Russian language journals in our review. We could incorporate articles published in French to our review, consulting reviews by Pampiglione [5, 6]. The last search was carried out on January 30, 2018.

In total, we found 99 cases of Dirofilaria affecting the maxillo-mandibular region in literature and the present case is the 100th one.

Results and Discussion

The habitual hosts are infected after a bite by various arthropods which are biological carriers and serve as intermediate hosts and can transmit it to humans during their subsequent meals [7]. In India, dog population is estimated to be around 25 million [8] An Indian study from Southern India reported blood smear from 7.59% of dogs to be positive for Dirofilaria [9]. In another survey, 16.7% of dogs in Mumbai were shown to be infected with Dirofilaria repens and 4.5% of dogs in Delhi were infected with Dirofilaria immitis [10]. This suggests that humans are at a higher risk of acquiring Dirofilaria infection from dogs.

Humans are the dead-end host where Dirofilaria develops into an unmated worm that neither reproduces nor releases microfilariae. Human-to-human and human-to-arthropod transmission, thus does not occur [7]. Dirofilaria reaches human through an insect bite that mostly cannot be recalled by patient and sometimes bite may be recalled as painful followed by slight local acute phlogosis (erythema, swelling and pruritis) lasting for few days. Dirofilaria may even invade the blood stream and may be carried to distant sites like lungs, genitalia, omentum. Finally, Dirofilaria dies and mounts a severe foreign body response and forms nodules which may even suppurate, and the signs and symptoms are in accordance with the site of entrapment.

The first reported case of dirofilariasis was in subconjunctival region in France in a 3-year-old female in 1566. Since then more than 800 cases have been reported, and dirofilariasis is considered as an emerging zoonosis [11, 12]. In this review, we analyzed only the cases of dirofilariasis involving the maxillo-mandibular region and characterized them with regard to geographic, age, gender and affected site distribution. The first reported case of maxillo-mandibular dirofilariasis was in year 1864 in a 20-year-old male patient affecting the lip [13]. There are total 100 reported cases of maxillo-mandibular dirofilariasis till now including the present case. (Table 1). There were barely a few reported cases of maxillo-mandibular dirofilariasis before 1980. After that, there was a sharp increase in the reported cases over the next two decades followed by gradual fall over the next two decades. The maximum number of reported cases was in the time frame of 1991–2000 (31 cases) (Fig. 5). The reason for initial increase in all probability is multifactorial. At least a part of increase in the incidence of the disease may be attributed to the changing climatic conditions (temperature, relative humidity, rainfall and evaporation) that favor the growth of the carrier culicidae and also the development of larval phase of nematode inside the carrier [14, 15]. Further, it has been postulated that greenhouse effect has further increased the vector population globally causing an increase in vector-borne diseases like malaria, dengue, and dirofilariasis [16].

Table 1.

Area wise distribution

S.NO Reporting Author/ Ref Year Age/Sex Site
India
1 Senthilvel [17] 1999 39/F Lip
2 Padmaja [18] 2005 35/F Lip
3 Khurana [19] 2010 45/M cheek
4 Joseph [20] 2010 10/F Nasolabial
5 Joseph [20] 2010 39/F Parotid
6 Joseph [20] 2010 24/F Infraorbital
7 Joseph [20] 2010 45/F Cheek
8 Permi [21] 2011 40/M Cheek
9 Souza [22] 2013 28/M Cheek
10 Nath [23] 2013 30/M Cheek
11 Kurup [1] 2013 54/F Buccal mucosa
12 Khyriem [24] 2013 27/F Cheek
13 Manuel [25] 2014 32/M Buccal vestibule
14 Janardhanan [26] 2014 54/F cheek
15 Premakumar [27] 2014 32/M Cheek
16 Krishna [28] 2015 64/F Infraorbital
17 Desai [29] 2015 32/M Buccal mucosa
18 Balaji [30] 2016 19/F Buccal mucosa
19 Present case 2017 26/M Retromolar area
Sri Lanka
20 Attygalle [31] 1966 48/M Parotid region
21 Dissanaike [32] 1997 3/M Cheek
22 Dissanaike [32] 1997 10 m/F Cheek
23 Dissanaike [32] 1997 28/M Cheek
24 Ratnatunga [33] 1999 65/F Cheek
25 Ratnatunga [33] 1999 45/M Cheek
26 Pitakotuwage [34] 1999 80/F Cheek
27 Tilakaratne [35] 2003 26/F Buccal mucosa
28 Tilakaratne [35] 2003 80/F Buccal mucosa
29 Tilakaratne [35] 2003 52/F Buccal mucosa
30 Tilakaratne [35] 2003 28/F Buccal mucosa
31 Tilakaratne [35] 2003 4/F Buccal mucosa
32 Tilakaratne [35] 2003 40/F Buccal mucosa
33 Tilakaratne [35] 2003 53/M Lip
34 Jayasinghe [36] 2011 57/F Cheek
35 Jayasinghe [36] 2011 20/M Cheek
36 Senanayke [37] 2013 11 M/NS Cheek
Italy
37 Pane [13] 1864 20/M Lip
38 Babudiere [5] 1937 18/M Cheek
39 Colla [5] 1967 71/M Cheek
40 Colla [5] 1967 54/F Cheek
41 Bianchi [5] 1968 20/M Zygomatic
42 Fruttaldo [5] 1985 40/M Zygomatic
43 Fruttaldo [5] 1985 44/M Zygomatic
44 Toniolo [5] 1987 23/M Jaw
45 Bertiato [5] 1987 25/M Mandibular
46 Pampiglione [5] 1988 37/F Cheek
47 Pampiglione [38] 1993 53/M lip
48 Maccioni [5] 1994 38/M Zygomatic
49 Pampiglione [6] 1996 38/M Zygomatic
50 Pampiglione [39] 1996 43/F Temporalis
51 Cancirini [40] 1998 59/M Submandibular lymph node
52 Pampiglione [6] 1999 39/M Zygomatic
53 Pampiglione [6] 1999 27/F Cheek
54 Pampiglione [6] 1999 4/M Cheek
Russia
55 Maximova [41] 1991 41/F Zygomatic
56 Avdiukhina [3] 1993 35/M Submandibular
57 Postnova [42] 1997 33/F Cheek
58 Postnova [42] 1997 31/M Cheek
59 Postnova [42] 1997 18/F Cheek
60 Postnova [42] 1997 35/F Soft palate
61 Avdiukhina [3] 1997 55/F Lip
62 Laura [43] 2007 23/F Oral cavity
63 Laura [43] 2007 43/F Cheek
64 Ilyasov [4] 2014 32/F Cheek
65 Ilyasov [4] 2014 38/F Zygomatic
66 Ilyasov [4] 2014 30/F Parotid
Greece
67 Triantafillopoulos [44] 1952 26/F Cheek
68 Markopoulos [45] 1990 48/F Cheek
69 Auer [46] 1997 NS Parotid
70 Tzanetou [47] 2009 45/F Cheek
France
71 Quilici [5] 1982 35/F Zygomatic
72 Quicili [5] 1983 19/M Cheek
73 Lapierre [48] 1982 42/M Cheek
74 Quicili [5] 1986 50/M Zygomatic
75 Quicili [5] 1987 47/M Cheek
76 Quicili [5] 1991 38/F Zygomatic
77 Quicili [5] 1993 29/M Cheek
78 Quicili [5] 1993 56/M Cheek
79 Weill [6] 1999 66/M Cheek
80 AbouBacar [49] 2007 35/M Cheek
81 Rivière [50] 2014 52/F Intramasseteric
Turkey
82 Latifoğlu [2] 2002 62/M Premasseteric mass
China
83 Tsang [51] 2003 42/F Buccal mucosa
Britain
84 Seddon [52] 1992 12/M Parotid
85 Ahmed [53] 2010 32/M Parotid
Tunisia
86 Kaouech [54] 2010 40/F Lip
Germany
87 Friedrich [55]  2014 40/F Zygomaticotemporal
Brazil
88 Pereira [56] 2015 65/F Buccal mucosa
89 Daroit [57] 2016 65/F Buccal mucosa
United States of America
90 Collins BM [58] 1992 53/M Cheek
91 AJ Herzberg [59] 1995 66/M Cheek
92 Akst LM [60] 2004 73/F Cheek
93 VélezPérez [61] 2016 79/M Buccal mucosa
Iran
94 Maraghi [62] 2006 34/M Cheek
95 Radmanesh [63] 2006 31/M Nasolabial
Austria
96 Fuehrer [64] 2000 59/M Cheek
97 Fuehrer [64] 2008 62/F Cheek
98 Barbara Bockie [65] 2009 52/M Cheek
Ukraine
99 Enghelestein [66] 1973 17/F Submandibular
Georgia
100 Zenaishvili [5] 1983 28/F Tongue
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Clinical diagnosis of dirofilariasis is almost wrong and is usually mistaken for malignancy, cyst, adenoma, hematoma, lipoma, abscess and a wide range of differentials except dirofilariasis. Jelink et al. [67] reported two patients feeling “worm under skin” who were wrongly admitted in psychiatry ward and were later on diagnosed with Dirofilaria. Similarly, one patient was diagnosed with trigeminal neuralgia and was completely relieved after nematode was removed from the bulbar conjunctiva, and it was probably due to Dirofilaria migration to the head [3].

Radical surgeries were thus performed and later on histopathologically diagnosed it to be Dirofilaria. This has led to an increased interest among academicians resulting in greater reporting, hence further increasing the total evidence in the form of published data. Thus, the increase may have been an indirect result of increased awareness among medical practitioners about Dirofilaria. Technical advancements and increased availability of refined diagnostic aids like use of PAS and Masson–Goldner’s trichrome stains and use of biomolecular techniques like PCR assay for phylogenetic analysis further increased the case detection [68]. Thereafter, gradual decrease in reported cases over the last two decades (26 cases in 2001–2010 and 23 in the present decade) could have been due to better vector control.

Previous reviews of dirofilariasis of whole body have shown it to be an endemic disease of primarily third world temperate countries like Italy, France, Russia and Sri Lanka. In the present review also, this holds true as we have found 62 cases in temperate region and 38 cases in tropical countries. Interestingly the number of cases in the tropical countries is increasing significantly over the last 40 years. On the other hand, reported number of cases in temperate countries is showing a sharp downward trend for the last 3 decades. This virtual shift could also be related partly to control of canine vector-borne diseases in European countries (temperate climate). WHO in 2015 has declared Europe malaria-free with one of its modalities being mosquito control [69]. This vector control could have resulted in decline in cases in last two decades in European countries where earlier it was quite rampant. However europe being declared as malaria free due to vector control and its exact influence on incidence of dirofilaria in europe, still needs to be studied better. Our study reflects that India (19%) has topped the list followed by Italy (18%) and Sri Lanka (17%) in the reported number of cases which could be credited to wide range of climatic conditions, huge population density, large rural population, lack of personal hygiene, reduced availability of preventive health-care facilities, abundance of stray animals and vectors, reduced education, awareness among masses and reduced veterinary facilities.

Age distribution of dirofilariasis shows that it can affect any age group. In our review of 100 patients with maxillo-mandibular dirofilariasis, mean age of occurrence is found to be 39.22 years, with a range from 10 months to 80 years. Maximum number of cases has been reported in the fourth decade of life followed by the third decade (Fig. 6). Female preponderance (51%) has been observed in the present review.

In the review published by Pampiglione et al. [6], only 3.4% of total body cases were from the maxillo-mandibular region. Involvement of maxillo-mandibular region is less common with involvement of the oral cavity being even rarer. In the present review, maximum number of cases were reported in cheek (45%) followed by buccal mucosa (13%) and then zygomaticotemporal region (12%). It seems that as these are the most prominent areas on the face for mosquito bite, Dirofilaria gets inoculated here, migrates and localizes in deeper tissues.

For the diagnosis of dirofilariasis, a suggestive patient history and clinical examination are important clues. Microscopic examination of the removed parasites or their fragments remains the golden standard to confirm the diagnosis. It becomes increasingly difficult for histopathologists to correctly diagnose the nematode when it is in the advanced stage of decomposition [70].

The definitive treatment of Dirofilaria infection in humans is surgical removal of the adult worm. If difficulty is encountered in surgical removal of the worm because of the excessive movement, a cryoprobe can be used for immobilizing it as described by Geldelman [71]. Medication such as diethylcarbamazine (DEC), ivermectin and albendazole is routinely administered. DEC (2 to 4 mg/kg body weight over a period of 4 weeks) is highly specific for microfilaria as it alters its membrane so that they are easily phagocytized by tissue-fixed monocytes. Albendazole is of adjuvant value in treating filariasis [72]. Ivermectin, a broad spectrum antiparasitic drug, blocks the transmission of microfilariae and can be administered as a single oral dose annually without any side effects [73].

Effective way of control of this parasitosis is basically adoption of proper vector control and increasing patient awareness. However, administrating prophylactic dose of ivermectin (> 6 µg/kg once a month for 7 consecutive months) to the canines in the endemic areas has also been proposed [73].

Conclusion

Although intraoral Dirofilaria infections are extremely uncommon, it should be considered in the differential diagnosis of an intraoral or facial swelling that does not completely respond to routine therapy especially in patients from endemic areas. This study was aimed toward an extensive data analysis of incidence, age distribution and country distribution of dirofilariasis in the world, so as to allow for a better understanding of pattern of maxillofacial dirofilariasis. In our opinion, there has not been much literature study in regard to maxillofacial dirofilariasis exclusively, making it a less likely candidate in differential diagnosis. The study aims to increase awareness of this amid medical professionals. Medical awareness of the risk of the infection is essential, and very often, a detailed history (including travel) is helpful in diagnosis. Many of them remain undiagnosed or unreported. Hence, it is emphasized that surgeon should have an increased awareness about this infection. This study could also serve to draw attention toward organized programs for elimination of the zoonotic disease from dogs and other reservoir hosts.

Conflict of interest

All authors declare that they have no conflict of interest.

Human and animal rights

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Contributor Information

Kirti Chaudhry, Email: chaudhry_kirti@yahoo.com.

Shruti Khatana, Phone: +91-7357552232, Phone: +91-7411165801, Email: shru.k85@gmail.com.

Naveen Dutt, Email: kirti_chaudhry@gmail.com.

Yogesh Mittal, Email: dryogesh82@gmail.com.

Shailja Sharma, Email: shailjachambial@yahoo.com.

Poonam Elhence, Email: drpoonamelhence@gmail.com.

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